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Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record

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Evolutionary Transitions to Multicellular Life

Part of the book series: Advances in Marine Genomics ((AMGE,volume 2))

Abstract

Developmental regulatory genes (largely transcription factors and signaling pathways) were once viewed as tightly connected to the origin of the morphological features with which they are associated in bilaterians. With the increased study of basal metazoans (sponges and cnidarians) as well as other eukaryotic clades, it is now clear that many of these highly conserved genes arose much earlier in evolution, and served different biological purposes. This provides a new view of the nature of developmental toolkits associated with the early origin of Metazoa: ancient regulatory genes were only later co-opted for the various developmental roles associated with bilaterian morphology. Here we review the nature of the toolkits at the origin of Metazoa, the Placozoan-Eumetazoan last common ancestor (LCA), the Cnidarian-Bilaterian LCA, and the Protostome-Deuterostome LCA. Integrating this data with recent molecular clock results and data on the fossil record reveals long macroevolutionary lags between the origin of the molecular toolkits and their developmental potential, and the origin of crown group morphologies as documented in the fossil record.

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References

  • Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2(10):e1031

    Google Scholar 

  • Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12(5):494–518

    CAS  Google Scholar 

  • Adamska M, Degnan BM, Green K, Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114(1):1–10

    Google Scholar 

  • Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    CAS  Google Scholar 

  • Arendt D (2008) The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9:868–883

    CAS  Google Scholar 

  • Arendt D, Nubler-Jung K (1994) Inversion of dorso-ventral axis. Nature 371:26

    CAS  Google Scholar 

  • Arendt D, Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Proc R Soc Lond B Biol Sci 356:1545–1563

    CAS  Google Scholar 

  • Backfisch B, Rajan VBV, Fischer RM, Lohs C, Arboleda E, Tessmar-Raible K, Raible F (2013) Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proc Natl Acad Sci U S A 110(1):193–198

    CAS  Google Scholar 

  • Baguñà J, Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Riutort M (2001) The first bilaterian organisms: simple or complex? New molecular evidence. Int J Dev Biol 45(S1):S133–S134

    Google Scholar 

  • Baguñà J, Martinez P, Paps J, Riutort M (2008) Back in time: a new systematic proposal for the Bilateria. Philos Trans R Soc Lond B Biol Sci 363:1481–1491

    Google Scholar 

  • Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907–2916

    CAS  Google Scholar 

  • Callaerts P, Halder G, Gehring WJ (1997) Pax-6 in development and evolution. Annu Rev Neurosci 20:483–532

    CAS  Google Scholar 

  • Caestro C, Bassham S, Postlethwait J (2005) Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev Biol 285(2):298–315

    Google Scholar 

  • Carroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity. Blackwell Science, Malden

    Google Scholar 

  • Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkock C, Sumin N, Sutton GG, Devi Viswanathan L, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang J-S, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PRH, Zhang X, Aufschnaiter R, Eder M-F, Gorny A-K, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Böttger A, Tishler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TCG, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE (2010) The dynamic genome of Hydra. Nature 464:592–597

    CAS  Google Scholar 

  • Chiori R, Jager M, Denker E, Wincker P, Da Silva C, Le Guyader H, Manuel M, Quéinnec E (2009) Are Hox genes ancestrally involved in axial patterning? Evidence from the Hydrozoan Clytia hemisphaerica (Cnidaria). PLoS One 4(1):e4231

    Google Scholar 

  • Davidson EH, Erwin DH (2010) An integrated view of Precambrian eumetazoan evolution. Cold Spring Harb Symp Quant Biol 79:65–80

    Google Scholar 

  • De RobertisEM(2008) Evo-Devo: variations on ancestral patterning in bilateria. Nature 380:37–40

    Google Scholar 

  • De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308

    CAS  Google Scholar 

  • De Robertis EM, Sasai Y (1996) A common plan for dorsoventral patterning in bilateria. Nature 380:37–40

    CAS  Google Scholar 

  • Dray N, Tessmar-Raible K, Le Gouar M, Vibert L, Christodoulou F, Schipany K, Guillou A, Zantke J, Snyman H, Béhague J (2010) Hedgehog signaling regulates segment formation in the annelid Platynereis. Science 329(5989):339–342

    CAS  Google Scholar 

  • Edgecombe GD, Giribet G, Dunn CW, Hejnol A, Kristensen RM, Neves RC, Rouse GW, Worsaae K, Sørensen MV (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172

    Google Scholar 

  • Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction, and diversity. Trends Ecol Evol 23:304–310

    Google Scholar 

  • Erwin, DH (2009) Early origin of the bilaterian developmental toolkit. Philos Trans R Soc Lond B Biol Sci 364:2253–2261

    CAS  Google Scholar 

  • Erwin DH, Davidson EH (2002) The last common bilaterian ancestor. Development 129(13): 3021–3032

    CAS  Google Scholar 

  • Erwin DH, Valentine JW (2013) The cambrian explosion: the construction of animal biodiversity. Roberts & Co., Greenwood

    Google Scholar 

  • Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ (2011) The Cambrian Conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091–1097

    CAS  Google Scholar 

  • Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617

    CAS  Google Scholar 

  • Fahey B, Larroux C, Woodcroft BJ, Degnan BM (2008) Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 214(3):205–217

    CAS  Google Scholar 

  • Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, Manning G, Lang BF, Haas B, Nusbaum C, King N (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:R15

    Google Scholar 

  • Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304:1335–1337

    CAS  Google Scholar 

  • Forêt S, Knack B, Houliston E, Momose T, Manuel M, Quéinnec E, Hayward DC, Ball E, Miller DJ (2010) New tricks with old genes: the genetic basis of novel cnidarian traits. Trends Genet 26(4):154–158

    Google Scholar 

  • Fortunato S, Adamski M, Bergum B, Guder C, Jordal S, Leininger S, Zwafink C, Rapp HT, Adamska M (2012) Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns. EvoDevo 3:14

    CAS  Google Scholar 

  • Fritz AE, Ikmi A, Seidel C, Paulson A, Gibson MC (2013) Mechanisms of tentacle morphogenesis in the sea anemone Nematostella vectensis. Development 140:2212–2223

    CAS  Google Scholar 

  • Harcet M, Roller M, Cetkovic H, Peina D, Wiens M, Muller WE, Vlahovicek K (2010) Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans. Mol Biol Evol 27(12):2747–2756

    CAS  Google Scholar 

  • Hejnol A, Martindale MQ (2009) Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura. BMC Biol 7:65

    Google Scholar 

  • Holland PWH (2013) Evolution of homeobox genes. WIREs Dev Biol 2:31–45

    CAS  Google Scholar 

  • Hui JHL, Raible F, Korchagina N, Dray N, Samain S, Magdelenat G, Jubin C, Segurens B, Balavoine G, Arendt D, Ferrier DEK (2009) Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes. BMC Biol 7:43

    Google Scholar 

  • Ikuta T (2011) Evolution of invertebrate deuterostomes and Hox/ParaHox genes. Genomics Proteomics Bioinformatics 9(3):77–96

    CAS  Google Scholar 

  • Ingham P, Nakano Y, Seger C (2011) Mechanisms and functions of Hedgehog signaling across the metazoa. Nat Rev Genet 12:393–406

    CAS  Google Scholar 

  • Jablonski D, Bottjer DJ (1990) The origin and diversification of major groups: environmental patterns and macroevolutionary lags. In: Taylor PD, Larwood GP (eds) Major evolutionary radiations. Systematics association special, vol 42. Clarendon Press, Oxford, pp 17–57

    Google Scholar 

  • Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, Schierwater B (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214(4):170–175

    CAS  Google Scholar 

  • King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JGI, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783–788

    CAS  Google Scholar 

  • Knoll AH (2011) The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39:217–239

    CAS  Google Scholar 

  • Knoll AH, Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137

    CAS  Google Scholar 

  • Kraus Y, Fritzenwanker JH, Genikhovich G, Technau U (2007) The blastoporal organiser of a sea anemone. Curr Biol 17:R874–876

    CAS  Google Scholar 

  • Kuo D-H, Weisblat DA (2011) A new molecular logic for BMP-mediated dorsoventral patterning in the leech Helobdella. Curr Biol 21:1281–1288

    Google Scholar 

  • Larroux C, Luke GN, Koopman P, Rohksar D, Shimeld SM, Degnan BM (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25:980–996

    CAS  Google Scholar 

  • Lee PN, Kumburegama S, Marlow HQ, Martindale MQ, Wikramanayake AH (2007) Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. Dev Biol 310:169–186

    CAS  Google Scholar 

  • Leys SP, Riesgo A (2012) Epithelia, an evolutionary novelty of metazoans. J Exp Zool B Mol Dev Evol 318(6):438–447

    Google Scholar 

  • Leys SP, Cronin TW, Degnan BM, Marshall JN (2002) Spectral sensitivity in a sponge larva. J Comp Physiol A 188:199–202

    Google Scholar 

  • Love GD, Grosjean E, Stalvie C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of Demospongia during the Cryogenian period. Nature 457:718–721

    CAS  Google Scholar 

  • Lowe CJ, Terasaki M, Wu M, Freeman RM Jr, Runft L, Kwan K, Haijo S, Aronowicz J, Lander E, Gruber C, Smith M, Kirschner M, Gerhart J (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4(9):e291

    Google Scholar 

  • Ma X, Hou X, Edgecombe GD, Strausfeld NJ (2012) Complex brain and optic lobes in an early Cambrian arthropod. Nature 490:258–263

    CAS  Google Scholar 

  • Magie CR, Pang K, Martindale MQ (2005) Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev Genes Evol 215:618–630

    CAS  Google Scholar 

  • Maloof AC, Rose CV, Calmet CC, Beach R, Samuels BM, Erwin DH, Poirier GR, Yao N, Simons FJ (2010) Probable animal body-fossils from pre-Marinoan limestones, South Australia. Nat Geosci 3:653–659

    CAS  Google Scholar 

  • Martinelli C, Spring J (2008) Distinct expression patterns of the two T-box homologues Brachyury and Tbx2/3 in the placozoan Trichoplax adhaerens. Dev Genes Evol 213(10):492–499

    Google Scholar 

  • Maxwell EK, Ryan JF, Schnitzler CE, Browne WE, Baxevanis AD (2012) MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi. BMC Genomics 13:714

    CAS  Google Scholar 

  • Mayr E (1960) The emergence of novelty. In: Tax S (ed) The evolution of life. University of Chicago Press, Chicago, pp 349–380

    Google Scholar 

  • Miller DJ, Ball EE (2009) The gene complement of the ancestral bilaterian—was Urbilateria a monster? J Biol 8:89

    Google Scholar 

  • Momose T, Houliston E (2007) Two oppositely localized frizzled RNAs as axis determinants in a cnidarian embryo. PLoS Biol 5:e70

    Google Scholar 

  • Momose T, Derelle R, Houliston E (2008) A maternally localized Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 135:2105–2113

    CAS  Google Scholar 

  • Momose T, Kraus Y, Houliston E (2012) A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development. Development 139:4375–4382

    Google Scholar 

  • Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci U S A 103(33):12451–12456

    CAS  Google Scholar 

  • Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N (2012) Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/beta-catenin complex. Proc Natl Acad Sci U S A 109(32):13046–13051

    CAS  Google Scholar 

  • Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Muller WEG, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G. (2013) Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67:223–233

    Google Scholar 

  • Ogura A, Ikeo K, Gojobori T (2005) Estimation of ancestral gene set of bilaterian animals and its implication to dynamic change of gene content in bilaterian evolution. Gene 345(1):65–71

    CAS  Google Scholar 

  • Pang K, Ryan JF, Baxevanis AD, Martindale MQ (2011) Evolution of the TGF-beta signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS One 6(9):e24152

    CAS  Google Scholar 

  • Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signaling centres. Nature 483:289–296

    CAS  Google Scholar 

  • Parfrey LM, Lahr DJG (2013) Multicellularity arose several times in the evolution of eukaryotes. Bioessays 35:339–347

    CAS  Google Scholar 

  • Petersen CP, Reddien PW (2009) Wnt signaling and the polarity of the primary body axis. Cell 139:1056–1068

    CAS  Google Scholar 

  • Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ (2011a) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258

    Google Scholar 

  • Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D (2011b) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9(3):e1000602

    Google Scholar 

  • Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–96

    Google Scholar 

  • Ramos OM, Barker D, Ferrier DEK (2012) Ghost loci imply Hox and ParaHox existence in the last common ancestor of animals. Curr Biol 22:1951–1956

    Google Scholar 

  • Richards GS, Degnan BM (2012) The expression of Delta ligands in the sponge Amphimedon queenslandica suggest an ancient role for Notch signaling in metazoan development. EvoDevo 3:1–15

    Google Scholar 

  • Ringrose JH, van den Toorn HWP, Eitel M, Post H, Neerincx P, Schierwater B, Altelaar AFM, Heck AJR (2013) Deep proteome profiling of Trichoplax adhaerens reveals remarkable features at the origin of metazoan multicellularity. Nat Commun 4(1408):1–7

    Google Scholar 

  • Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM, Sancar A, Oakley TH (2012) Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J Exp Biol 215:1278–1286

    CAS  Google Scholar 

  • Rivera A, Winters I, Rued A, Ding S, Posfai D, Cieniewicz B, Cameron K, Gentile L, Hill A (2013) The evolution and function of the Pax/Six regulatory network in sponges. Evol Dev 15(3):186–196

    CAS  Google Scholar 

  • Robinson JM, Sperling EA, Bergum B, Adamski M, Nichols SA, Adamska M, Peterson KJ (2013) The identification of microRNAs in Calcisponges: Independent eolution of microRNAs in basal metazoans. J Exp Zool B Mol Dev Evol 320:84–93

    Google Scholar 

  • Rokas A (2008) The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42:235–251

    CAS  Google Scholar 

  • Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for Ecdysozoan evolution. Curr Biol 23:392–398

    Google Scholar 

  • Röttinger E, Dahlin P, Martindale MQ (2012) A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specification: the inputs of β-catenin/TCF signaling. PLoS Genet 8(12):e1003164

    Google Scholar 

  • Rowland SJ (2001) Archaeocyaths—a history of phylogenetic interpretation. J Paleontol 75:1065–1078

    Google Scholar 

  • Ryan JF, Pang K, Mullikin JC, Martindale MQ, Baxevanis AD, Progra NCS (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo 1:9.

    Google Scholar 

  • Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, Smith SA, Putnam NH, Haddock SHD, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:124592

    Google Scholar 

  • Saina M, Genikhovich G, Renfer E, Technau U (2009) BMPs and Chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci U S A 106(44):18592–18597

    CAS  Google Scholar 

  • Schierwater B, Kamm K (2010) The early evolution of Hox genes: a battle of believe? In: Deutsch J (ed) Hox Genes’ studies from the 20th to the 21st century, advances in experimental medicine and biology, vol 689. Landes Bioscience, New York, pp 81–90

    Google Scholar 

  • Schierwater B, Eitel M, Osigus HJ, von der Chevallerie K, Bergmann T, Hadrys H, Cramm M, Heck L, Jakob W, Lang MR, DeSalle R (2011) Trichoplax and Placozoa: one of the crucial keys to understanding metazoan evolution. In: DeSalle R, Schierwater B (eds) Key transitions in animal evolution. Science Publishers, Enfield, pp 289–326

    Google Scholar 

  • Sebé-Pedrós A, Ruiz-Trillo I, de Mendoza A, Lang BF, Degnan BM (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28(3):1241–1254

    Google Scholar 

  • Sebé-Pedrós A, Ariza-Cosano A, Weirauch MT, Leininger S, Yang A, Torruella G, Adamski M, Adamska M, Hughes TR, Gómez-Skarmeta JL, Ruiz-Trillo I (2013) Early evolution of the T-box transcription factor family. Proc Natl Acad Sci U S A 110(40):16050–16055

    Google Scholar 

  • Shenk MA, Steel MA (1994) A molecular snapshot of the metazoan ‘Eve’. Trends Biochem Sci 18:459–463

    Google Scholar 

  • Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, Grigoriev IV, Lindberg DR, Seaver EC, Weisblat DA, Putnam NH, Rokhsar DS (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–532

    CAS  Google Scholar 

  • Sinigaglia C, Busengdal H, Leclère L, Technau U, Rentzsch F (2013) The bilaterian head patterning gene six3/6 controls aboral domain development in a cnidarian. PLoS Biol 11(2):e1001488

    CAS  Google Scholar 

  • Sperling EA, Vinther J (2010) A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol Dev 12:201–209

    Google Scholar 

  • Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and its implications for Precambrian palaeobiology. In: Vickers-Rich P, Komarower P (eds) The rise and fall of the Ediacaran biota, geological society special publication, vol 286. Geological Society of London, London, pp 355–368

    Google Scholar 

  • Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of eumetazoa. Mol Biol Evol 26:2261–2274

    CAS  Google Scholar 

  • Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454(7207):955–960

    CAS  Google Scholar 

  • Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS (2010a) Early evolution of the LIM homeobox gene family. BMC Biol 8(4):1–13

    Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai YF, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu SQ, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010b) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–723

    Google Scholar 

  • Steele RE, David CN, Technau U (2011) A genomic view of 500 million years of cnidarian evolution. Trends Genet 27(1):7–13

    CAS  Google Scholar 

  • Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Wörheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487(7406):231–234

    CAS  Google Scholar 

  • Stromberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proc Natl Acad Sci U S A 102:11980–11984

    Google Scholar 

  • Sullivan JC, Kalaitzidis D, Gilmore TD, Finnerty JR (2006) Rel homology domain-containing transcription factors in the cnidarian Nematostella vectensis. Dev Genes Evol 217:63–72

    Google Scholar 

  • Valentine JW, Jablonski D, Erwin DH (1999) Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126:851–859

    CAS  Google Scholar 

  • Vij S, Rink JC, Ho HK, Babu D, Eitel M, Narasimhan V, Tiku V, Westbrook J, Schierwater B, Roy S (2012) Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS Genet 8(11):e1003019

    CAS  Google Scholar 

  • Winchell CJ, Jacobs DK (2013) Expression of the Lhx genes apterous and lim1 in an errant polychaete: implications for bilaterian appendage evolution, neural development, and muscle diversification. EvoDevo 4:4

    CAS  Google Scholar 

  • Winchell CJ, Valencia JE, Jacobs DK (2010) Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata Annedlida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria. Dev Genes Evol 220:275–295

    Google Scholar 

  • Windsor PJ, Leys SP (2010) Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer. Evol Dev 12(5):484–493

    CAS  Google Scholar 

  • Wyder S, Kriventseva EV, Schröder R, Kadowaki T, Zdobnov EM (2007) Quantification of ortholog losses in insects and vertebrates. Genome Biol 8(11):R242

    Google Scholar 

  • Xavier-Neto J, Castro RA, Sampaio AC, Azambuja AP, Castillo HA, Cravo RM, Simões-Costa MS (2007) Parallel avenues in the evolution of hearts and pumping organs. Cell Mol Life Sci 64:719–734

    CAS  Google Scholar 

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Acknowledgment

SMT and DHE acknowledge financial support from a NASA Astrobiology Institute grant (MIT node; to DHE).

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Correspondence to Sarah M. Tweedt .

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Tweedt, S., Erwin, D. (2015). Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record. In: Ruiz-Trillo, I., Nedelcu, A. (eds) Evolutionary Transitions to Multicellular Life. Advances in Marine Genomics, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9642-2_3

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